Stabilizing Exposure of Conserved Epitopes by Structure Guided Insertion of Disulfide Bond in HIV-1 Envelope Glycoprotein

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Kassa, Aemro ^a,e   Dey, Antu K ^a   Sarkar, Pampi ^a   Labranche, Celia ^c   Go, Eden P ^d   Clark, Daniel F ^d   Sun, Yide ^b   Nandi, Avishek ^a   Hartog, Karin ^b   Desaire, Heather ^d   Montefiori, David ^c   Carfi, Andrea ^a   Srivastava, Indresh K ^a,f   Barnett, Susan W ^a  

^a Novartis Vaccines and Diagnostics Inc   (United States)

^b Novartis Vaccines and Diagnostics Inc   (United States)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

^d UNIVERSITY OF KANSAS   (United States)

^e BOEHRINGER INGELHEIM PHARMA GMBH AND CO KG   (Germany)

^f Protein Sciences Corp   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; GLYCOPROTEIN GP 120; GLYCOPROTEIN GP 140;

AMINO ACID SUBSTITUTION; ANIMAL EXPERIMENT; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ANTIGEN BINDING; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DISSOCIATION CONSTANT; DISULFIDE BOND; FEMALE; IMMUNOGENICITY; LIGAND BINDING; NONHUMAN; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN PURIFICATION; RECEPTOR BINDING; STRUCTURE ANALYSIS; SURFACE PLASMON RESONANCE; VIRUS NEUTRALIZATION; WILD TYPE;

ANIMALS; ANTIBODIES; ANTIGENS, CD4; BINDING SITES; DISULFIDES; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; EPITOPES; FEMALE; HIV ENVELOPE PROTEIN GP120; HIV-1; HUMANS; IMMUNIZATION; LIGANDS; MODELS, MOLECULAR; MUTATION; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; RABBITS; SURFACE PLASMON RESONANCE;

EID: 84885706453     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0076139     Document Type: Article

References (54)

1. Allaway GP, Davis-Bruno KL, Beaudry GA, Garcia EB, Wong EL, et al. (1995) Expression and characterization of CD4-IgG2, a novel heterotetramer that neutralizes primary HIV type 1 isolates. AIDS Res Hum Retroviruses 11: 533-539.
2. (2010) Global Report: UNAIDS report on the global AIDS epidemic.
3. Scheid JF, Mouquet H, Feldhahn N, Seaman MS, Velinzon K, et al. (2009) Broad diversity of neutralizing antibodies isolated from memory B cells in HIV-infected individuals. Nature 458: 636-640.
4. Kwong PD, Doyle ML, Casper DJ, Cicala C, Leavitt SA, et al. (2002) HIV-1 evades antibody-mediated neutralization through conformational masking of receptor-binding sites. Nature 420: 678-682.
5. Kwon YD, Finzi A, Wu X, Dogo-Isonagie C, Lee LK, et al. (2012) Unliganded HIV-1 gp120 core structures assume the CD4-bound conformation with regulation by quaternary interactions and variable loops. Proc Natl Acad Sci U S A 109: 5663-5668.
6. Pancera M, Majeed S, Ban YE, Chen L, Huang CC, et al. (2010) Structure of HIV-1 gp120 with gp41-interactive region reveals layered envelope architecture and basis of conformational mobility. Proc Natl Acad Sci U S A 107: 1166-1171.
7. Kwong PD, Wyatt R, Robinson J, Sweet RW, Sodroski J, et al. (1998) Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393: 648-659.
8. Wyatt R, Kwong PD, Desjardins E, Sweet RW, Robinson J, et al. (1998) The antigenic structure of the HIV gp120 envelope glycoprotein. Nature 393: 705-711.
9. Huang CC, Tang M, Zhang MY, Majeed S, Montabana E, et al. (2005) Structure of a V3-containing HIV-1 gp120 core. Science 310: 1025-1028.
10. Kwong PD, Wyatt R, Majeed S, Robinson J, Sweet RW, et al. (2000) Structures of HIV-1 gp120 envelope glycoproteins from laboratory-adapted and primary isolates. Structure 8: 1329-1339.
11. Kassa A, Madani N, Schon A, Haim H, Finzi A, et al. (2009) Transitions to and from the CD4-bound conformation are modulated by a single-residue change in the human immunodeficiency virus type 1 gp120 inner domain. J Virol 83: 8364-8378.
12. Finzi A, Xiang SH, Pacheco B, Wang L, Haight J, et al. (2010) Topological layers in the HIV-1 gp120 inner domain regulate gp41 interaction and CD4-triggered conformational transitions. Mol Cell 37: 656-667.
13. Kwong PD, (2005) Human immunodeficiency virus: refolding the envelope. Nature 433: 815-816.
14. Chen B, Vogan EM, Gong H, Skehel JJ, Wiley DC, et al. (2005) Structure of an unliganded simian immunodeficiency virus gp120 core. Nature 433: 834-841.
15. Kassa A, Finzi A, Pancera M, Courter JR, Smith AB, (2009) Identification of a human immunodeficiency virus type 1 envelope glycoprotein variant resistant to cold inactivation. J Virol 83: 4476-4488.
16. Dey B, Svehla K, Xu L, Wycuff D, Zhou T, et al. (2009) Structure-based stabilization of HIV-1 gp120 enhances humoral immune responses to the induced co-receptor binding site. PLoS Pathog 5: e1000445.
17. Zhou T, Xu L, Dey B, Hessell AJ, Van Ryk D, et al. (2007) Structural definition of a conserved neutralization epitope on HIV-1 gp120. Nature 445: 732-737.
18. Chen L, Kwon YD, Zhou T, Wu X, O'Dell S, et al. (2009) Structural basis of immune evasion at the site of CD4 attachment on HIV-1 gp120. Science 326: 1123-1127.
19. Srivastava IK, Stamatatos L, Kan E, Vajdy M, Lian Y, et al. (2003) Purification, characterization, and immunogenicity of a soluble trimeric envelope protein containing a partial deletion of the V2 loop derived from SF162, an R5-tropic human immunodeficiency virus type 1 isolate. J Virol 77: 11244-11259.
20. Srivastava IK, Kan E, Sun Y, Sharma VA, Cisto J, et al. (2008) Comparative evaluation of trimeric envelope glycoproteins derived from subtype C and B HIV-1 R5 isolates. Virology 372: 273-290.
21. Dey AK, Khati M, Tang M, Wyatt R, Lea SM, et al. (2005) An aptamer that neutralizes R5 strains of human immunodeficiency virus type 1 blocks gp120-CCR5 interaction. J Virol 79: 13806-13810.
22. Yu B, Fonseca DP, O'Rourke SM, Berman PW, (2010) Protease cleavage sites in HIV-1 gp120 recognized by antigen processing enzymes are conserved and located at receptor binding sites. J Virol 84: 1513-1526.
23. Yu B, Morales JF, O'Rourke SM, Tatsuno GP, Berman PW, (2012) Glycoform and net charge heterogeneity in gp120 immunogens used in HIV vaccine trials. PLoS One 7: e43903.
24. Dey AK, Burke B, Sun Y, Hartog K, Heeney JL, et al. (2012) Use of a polyanionic carbomer, Carbopol971P, in combination with MF59, improves antibody responses to HIV-1 envelope glycoprotein. Vaccine 30: 2749-2759.
25. Thali M, Olshevsky U, Furman C, Gabuzda D, Li J, et al. (1991) Effects of changes in gp120-CD4 binding affinity on human immunodeficiency virus type 1 envelope glycoprotein function and soluble CD4 sensitivity. J Virol 65: 5007-5012.
26. Thali M, Olshevsky U, Furman C, Gabuzda D, Posner M, et al. (1991) Characterization of a discontinuous human immunodeficiency virus type 1 gp120 epitope recognized by a broadly reactive neutralizing human monoclonal antibody. J Virol 65: 6188-6193.
27. Li Y, Svehla K, Louder MK, Wycuff D, Phogat S, et al. (2009) Analysis of neutralization specificities in polyclonal sera derived from human immunodeficiency virus type 1-infected individuals. J Virol 83: 1045-1059.
28. Dey AK, Burke B, Sun Y, Sirokman K, Nandi A, et al. (2012) Elicitation of neutralizing antibodies directed against CD4-induced epitope(s) using a CD4 mimetic cross-linked to a HIV-1 envelope glycoprotein. PLoS One 7: e30233.
29. Xiang SH, Doka N, Choudhary RK, Sodroski J, Robinson JE, (2002) Characterization of CD4-induced epitopes on the HIV type 1 gp120 envelope glycoprotein recognized by neutralizing human monoclonal antibodies. AIDS Res Hum Retroviruses 18: 1207-1217.
30. Kovacs JM, Nkolola JP, Penga H, Cheung A, Perry J, et al. (2012) HIV-1 envelope trimer elicits more potent neutralizing antibody responses than monomeric gp120. Proc Natl Acad Sci USA(in press).
31. Beddows S, Franti M, Dey AK, Kirschner M, Iyer SP, et al. (2007) A comparative immunogenicity study in rabbits of disulfide-stabilized, proteolytically cleaved, soluble trimeric human immunodeficiency virus type 1 gp140, trimeric cleavage-defective gp140 and monomeric gp120. Virology 360: 329-340.
32. Zhang PF, Cham F, Dong M, Choudhary A, Bouma P, et al. (2007) Extensively cross-reactive anti-HIV-1 neutralizing antibodies induced by gp140 immunization. Proc Natl Acad Sci U S A 104: 10193-10198.
33. Dey B, Pancera M, Svehla K, Shu Y, Xiang SH, et al. (2007) Characterization of human immunodeficiency virus type 1 monomeric and trimeric gp120 glycoproteins stabilized in the CD4-bound state: antigenicity, biophysics, and immunogenicity. J Virol 81: 5579-5593.
34. Forsell MN, (2009) Schief WR, Wyatt RT (2009) Immunogenicity of HIV-1 envelope glycoprotein oligomers. Curr Opin HIV AIDS 4: 380-387.
35. Wei X, Decker JM, Wang S, Hui H, Kappes JC, et al. (2003) Antibody neutralization and escape by HIV-1. Nature 422: 307-312.
36. Wyatt R, Sodroski J, (1998) The HIV-1 envelope glycoproteins: fusogens, antigens, and immunogens. Science 280: 1884-1888.
37. Myszka DG, Sweet RW, Hensley P, Brigham-Burke M, Kwong PD, et al. (2000) Energetics of the HIV gp120-CD4 binding reaction. Proc Natl Acad Sci U S A 97: 9026-9031.
38. Desormeaux A, Coutu M, Medjahed H, Pacheco B, Herschhorn A, et al. (2013) The Highly Conserved Layer-3 Component of the HIV-1 gp120 Inner Domain Is Critical for CD4-Required Conformational Transitions. J Virol 87: 2549-2562.
39. Go EP, Zhang Y, Menon S, Desaire H, (2011) Analysis of the disulfide bond arrangement of the HIV-1 envelope protein CON-S gp140 DeltaCFI shows variability in the V1 and V2 regions. J Proteome Res 10: 578-591.
40. Jobes DV, Daoust M, Nguyen V, Padua A, Michele S, et al. (2006) High incidence of unusual cysteine variants in gp120 envelope proteins from early HIV type 1 infections from a Phase 3 vaccine efficacy trial. AIDS Res Hum Retroviruses 22: 1014-1021.
41. DeVico A, Fouts T, Lewis GK, Gallo RC, Godfrey K, et al. (2007) Antibodies to CD4-induced sites in HIV gp120 correlate with the control of SHIV challenge in macaques vaccinated with subunit immunogens. Proc Natl Acad Sci U S A 104: 17477-17482.
42. Martin G, Burke B, Thai R, Dey AK, Combes O, et al. (2011) Stabilization of HIV-1 envelope in the CD4-bound conformation through specific crosslinking of a CD4 mimetic. J Biol Chem.
43. Vaine M, Wang S, Crooks ET, Jiang P, Montefiori DC, et al. (2008) Improved induction of antibodies against key neutralizing epitopes by human immunodeficiency virus type 1 gp120 DNA prime-protein boost vaccination compared to gp120 protein-only vaccination. J Virol 82: 7369-7378.
44. Crooks ET, Moore PL, Richman D, Robinson J, Crooks JA, et al. (2005) Characterizing anti-HIV monoclonal antibodies and immune sera by defining the mechanism of neutralization. Hum Antibodies 14: 101-113.
45. Binley JM, Lybarger EA, Crooks ET, Seaman MS, Gray E, et al. (2008) Profiling the specificity of neutralizing antibodies in a large panel of plasmas from patients chronically infected with human immunodeficiency virus type 1 subtypes B and C. J Virol. 82: 11651-11668.
46. Grundner C, Li Y, Louder M, Mascola J, Yang X, et al. (2005) Analysis of the neutralizing antibody response elicited in rabbits by repeated inoculation with trimeric HIV-1 envelope glycoproteins. Virology 331: 33-46.
47. Guan Y, Pazgier M, Sajadi MM, Kamin-Lewis R, Al-Darmarki S, et al. (2012) Diverse specificity and Q:1 effector function among human antibodies to HIV-1 envelope glycoprotein epitopes exposed by CD4 binding. Proc Natl Acad Sci U S A(in press).
48. Labrijn AF, Poignard P, Raja A, Zwick MB, Delgado K, et al. (2003) Access of antibody molecules to the conserved coreceptor binding site on glycoprotein gp120 is sterically restricted on primary human immunodeficiency virus type 1. J Virol 77: 10557-10565.
49. Huang CC, Stricher F, Martin L, Decker JM, Majeed S, et al. (2005) Scorpion-toxin mimics of CD4 in complex with human immunodeficiency virus gp120 crystal structures, molecular mimicry, and neutralization breadth. Structure 13: 755-768.
50. Guan Y, Pazgier M, Sajadi MM, Kamin-Lewis R, Al-Darmarki S, et al. (2013) Diverse specificity and effector function among human antibodies to HIV-1 envelope glycoprotein epitopes exposed by CD4 binding. Proc Natl Acad Sci U S A 110: E69-78.
51. Zhou T, Georgiev I, Wu X, Yang ZY, Dai K, et al. (2010) Structural basis for broad and potent neutralization of HIV-1 by antibody VRC01. Science 329: 811-817.
52. Srivastava IK, Stamatatos L, Legg H, Kan E, Fong A, et al. (2002) Purification and characterization of oligomeric envelope glycoprotein from a primary R5 subtype B human immunodeficiency virus. J Virol 76: 2835-2847.
53. Dey AK, David KB, Ray N, Ketas TJ, Klasse PJ, et al. (2008) N-terminal substitutions in HIV-1 gp41 reduce the expression of non-trimeric envelope glycoproteins on the virus. Virology 372: 187-200.
54. Dey AK, Burke B, Sun Y, Hartog H, Heeney JL, et al. (2012) Use of a polyanionic carbomer, Carbopol971P, in combination with MF59, improves antibody responses to HIV-1 envelope glycoprotein Manuscript under review.